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Historically, indoor air quality has been an issue in the industrial sector, where standards have been established to limit worker exposures to airborne contaminants. Only recently have we recognized poor indoor air quality as a broader public health problem that affects populations in office and institutional settings, in schools, and at home. At the American Legion convention in Philadelphia, the sentinel event resulted in 182 cases of pneumonia and 29 deaths caused by a previously unrecognized bacterium later dubbed Legionella pneumophilia.' The source of the bacterial exposure was ultimately determined to be the hotel's ventilation and humidification system. And so began the recognition of what now appears to be an epidemic of building-associated illness and disease.2 The scope of the indoor air quality problem is large, in terms of both the size of the population potentially at risk and the prevalence of symptoms and disease. Most Americans spend considerable portions of every day indoors. During much of the day, virtually all children ages 6 and older in the United States are in school, and younger children are increasingly in out-of-home day care. More than 50% of adult workers in North America and Western Europe are employed in "white collar" office settings.2 In this article, we describe the health problems caused by poor indoor air quality and how attention to the design, construction, maintenance, and repair of buildings can prevent further exposure and related disease.
HEALTH PROBLEMS ASSOCIATED WITH POLLUTED INDOOR AIR

include many indoor air contaminants such as house dust mites, cockroach allergens, molds, fungi, and environmental tobacco smoke.5 Other factors likely to cause or aggravate asthma include dust; irritant gases and vapors emitted from indoor furnishings or entrained (pulled in) from outside air; and more specific contaminants such as isocyanate-containing urethanes used for floor refinishing, in wood varnishes, and in paints. The increasing prevalence of asthma is particularly noticeable and troublesome among children and young adults. Data from the National Health Interview Survey show startling increases in self-reported asthma between 1980 and 1994.6 The estimated average annual rate per 1000 population for the total sampled rose from 30.7 in 1980 to 53.8 in 1993-1994. Rate increases were similar for males and females, for whites and African Americans, and for different age groups. Rates of physician office visits with asthma as the principal diagnosis increased overall from 21.4 per 1000 population in 1975 to 39.0 in
1995.

Poor indoor air quality can cause or contribute to the development of chronic diseases such as asthma, multiple chemical sensitivity, and hypersensitivity pneumonitis.2-4 In addition, it can cause a broader array of temporary conditions and symptoms such as headache, dry eyes, nasal congestion, nausea, and fatigue which, when they meet the clinical definition as discussed below, are referred to as "sick building syndrome." People who already have certain medical conditions such as asthma, allergies, and connective tissue disorders or are immunosuppressed by medications such as steroids or chemotherapeutic agents are at even greater risk than the general population.

Rates of asthma-related hospital admissions have also increased, although not as dramatically as prevalence.6 U.S. data from the National Hospital Discharge Survey for 1979-1994 reveal an overall increase in estimated average rates of hospitalization with asthma as the principal diagnosis. A rate of 17.6 per 10,000 population was observed in 1979-1980; the 1993-1994 rate was 18.1 per 10,000 population. Rates varied by age and gender. Among whites and those age 35 or older, rates actually decreased slightly. For African Americans and age groups younger than 35 years, rates increased. Data from the Underlying Cause of Death dataset for the time period 1960 to 1995 show a steady decline in death rates from asthma from 1960 through 1978, with an increasing trend thereafter from 8.2 per million in 1975-1978 to 17.9 per million in 1993-1995.6

Asthma. In the last two decades, a time when poor indoor air quality has been increasingly recognized as a potential health hazard, asthma has been increasing in prevalence and severity- both nationwide and internationally.> Indeed, identified risk factors for asthma
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P U B LI C H

Sick building syndrome. In sick building syndrome, symptoms are variable and may involve multiple systems of the body. Objective physical and laboratory findings may be limited. Characteristic, however, is the resolution of symptoms upon leaving the building and recurrence with reentry. Recognition of the problem by both medical and management personnel and identification of the source(s) of exposure often take considerable time. And multiple factors are usually operative. Common health complaints observed by investigators from the National Institute for Occupational Safety and Health in their evaluation of 529 buildings were "eye irritation, dry throat, headache, fatigue, sinus congestion, skin irritation, shortness of breath, cough, dizziness, nausea, sneezing, and nose irritation."7 One study of 4373 office workers from 42 different buildings found that the percentages with work-related
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sympto.-ms ranged from 5% for chest tightness to 68QY(, for lethargy.' Nasal
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of' respondents, 46%, and headache in.46%. The prevalence of symptoms varied somewhat with type of ventilation. Other investigators have reported similar symptom prevalence in epidemiologic studies of office workers, although Hoffman reported higher percentages of respiratory symptoms in hoth case and comparison groups of office workers in a study of building-related asthma in Colorado."" Although not strictly comparable, data from the 1994 National Health Interview Survey show a much lower prevalence in the general population of symptoms similar to those of sick building syndrome or conditions likely to be associated with poor indoor air.'' For example, 'Headache, excluding migraine" was reported by 1.6% of respondents ages 25 to 44, compared with 46% in bourge's study of office workers.'
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Multiple chemical sensitivity. Another "wake-up" call has been sounded by the emergence in the past two decades of a growing number of people with a disease known as multiple chemical sensitivity. '2 Originally
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described in the 1950s, multiple chemical sensitivity was viewed with skepticism by most mcdical practitioners until the 1980s and 1990s when it began to move into the mainstream of clinical practice. '1"4 The number of people in the United States with diagnosed multiple chemical sensitivity is unknown, but in a 1996 survey of 4000 adults in California carried out by the California Health Services Department, 6.3% of respondents reported a diagnosis of multiple chemical sensitivity. An additional 15.9% reported "chemical sensitivity" associated with multiple reactions, without a specific diagnosis of multiple chemical sensitivity.' Onset of the disease, characterized by multisystem response to low-level chemical exposures commonly encountered in the ambient environment, often follows exposures incurred in association with indoor air quality problems. For some, the development of multiple chemical sensitivity is preceded by symptoms of sick building syndrome. For a subset of the group with sick building syndrome, symptoms become persistent even when the individual is out of the work environment. Such persistence of symptoms is an indicator of increased risk for
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tems.3 The illness is characterized by flu-like symptoms that include fever, chills, fatigue, cough, chest tightness, and shortness of breath. Antibodies to causal organisms may be measurable in the peripheral blood. The disease is usually reversible if exposure does not continue. Over time, however, permanent changes including pulmonary fibrosis may result.
CAUSAL FACTORS
In 1989 the Director of NIOSH issued a report to Congress summarizing NIOSH's activities in the area of indoor air quality between 1971 and 1989.7 He reported that 0.5% of the 1200 Health Hazard Evaluations performed between 1971 and 1978 were for indoor air quality problems, compared with 12% for the period 19781980, with the proportion increasing to 20% per year in 1988 and early 1989. Health Hazard Evaluations are usually requested by workers or employers and thus are not necessarily representative of all buildings. Nevertheless, the number of buildings evaluated was large at 529, and included a variety of different building types. Government and business office buildings constituted 80%

the development of multiple chemical sensitivity. See above for the clinical definition of multiple chemical sensitivity.16 Symptoms are similar to those seen in sick building syndrome. While the physiology of multiple chemical sensitivity has not been clearly defined, it is generally believed that multiple chemical sensitivity occurs as a result of effects on the limbic system (part of the nervous system), the immune system, and the respiratory tract."2"3 In some cases, psychological factors appear to be operative in terms of onset and severity of illness both on individual and group levels. When the disease is work-related, it often occurs in long-term, dedicated, and hard-working employees. The increasing importance of multiple chemical sensitivity as a public health problem is attested to by the fact that it has now been recognized by the American Lung Association/American Thoracic Society, the American Public Health Association, the American Society of Heating, Refrigerating, and Air Conditioning Engineers (ASHRAE), the American Conference of Governmental Industrial Hygienists (ACGIH), and the U.S. Environmental Protection Agency (EPA), and the media has begun to focus on the needs of people with this condition.

of the total evaluated; schools and colleges, 13%; and health care facilities, 7%. NIOSH classified these building evaluations by the primary type of problem found:

Inadequate ventilation (53% of buildings examined). Causes of inadequate ventilation included not enough outdoor air, poor air distribution and mixing, air pressure differentials between offices, temperature and humidity extremes or unreasonable fluctuations or both, improper air filtration, and poor maintenance of ventilation systems.
Indoor air contaminants (15% of buildings examined). See Box on page 404 for a summary of indoor sources of air contaminants. The most common chemical culprits identified by NIOSH were volatile organic compounds (VOCs). These may be released (off-gas) from materials used in refinishing wood floors and trims; from chemicals used to dye draperies, upholstered furniture, and cloth coverings of cubicle partitions; from plywood used in interior construction or furniture; from carpets and carpet backings; from perfumes worn by building occupants; from cleaning agents used by custodial staff; from office equipment such as copiers; from office supplies such as certain processed paper, carbon paper, and carbonless paper; and from antimicrobial agents. In 4% of the buildings, it was the building materials themselves that provided the source of indoor air contamination. In addition to those described by NIOSH, other pollutants associated with poor indoor air quality include
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Hypersensitivity pneumonitis. Hypersensitivity pneumonitis was originally described in farm workers in association with exposure to thermophilic microorganisms in moldy hay.'7 Its appearance in association with indoor air in buildings and homes has been noted more recently. This condition can be caused by bacteria, fungi, and molds contaminating home humidifiers and building heating, ventilation, and air conditioning (HVAC) sys402

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also as dust collectors. Odors affect the comfort level of those exposed, draw attention to the environment, and may lower the threshold for effects of other air pollutants and climate variations.'8 Odors stem from a myriad of sources including VOCs from perfumes, copiers, and furniture materials as well as tobacco smoke, cooking processes, and cleaning products. Schools have their own particular sources of contaminants: chalk dust; fungi, bacteria, and viruses brought to the school environment by children and adults; and vapors and fumes from chemistry laboratories, wood1 ULi B LI C' 11

wash their hands, and more likely to share the "tools of the trade" such as pencils. Increasing the risk for adults in schools is their lack of resistance to viruses of childhood.

Outside air contamination (10% of buildings examined). Outdoor environmental pollutants may become part of the indoor air in buildings. These include, for example, pesticides, vehicular exhaust such as diesel exhaust from trucks at loading docks of commercial buildings, and tobacco smoke from smokers standing outside building entrances.
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Microbial contamination (5% of buildings examined). Water damage and pooling of water as a result of improper drainage of HVAC systems provide reservoirs for the growth of molds and fungi that in turn cause skin, respiratory tract, and in some cases systemic illness and disease. For example, molds such as Cladosporium, Penicillium, and Alternaria are commonly found as contaminants of improperly designed or maintained ventilation and humidification systems and in water-damaged walls, ceilings, and carpeting.'9 Unknown (13% of buildings examined). In 13% of cases, specific etiologic factors could not be identified by NIOSH.
Over the past 30 to 40 years, there has been an explosion in the number of chemicals produced and used in the manufacture of household and building products, including construction materials, interior refinishing materials, cleaning agents, furnishings, and office equipment and supplies. In addition, buildings and HVAC systems have deteriorated as a result of aging and inadequate maintenance or become obsolete as a result of technological advances. HVAC systems were redesigned in the 1970s to make them more energy efficient. The amount of fresh air being brought into buildings has been decreased in order to reduce the amount of energy needed to heat or cool it. Thus, there is less fresh air available to dilute indoor air contaminants. Maintenance and custodial practices have also changed over time, with more work performed during regular working hours instead of nights and weekends. The result is that building occupants are exposed during normal working hours to vapors from cleaning and polishing agents and dust generated by dusting, sweeping, and vacuuming.
RELATING CLINICAL FINDINGS TO INDOOR AIR QUALITY

Knowledge of specific etiologic factors is not necessary for symptomatic treatment of ill patients. However, cure and prevention do require knowledge of causal factors. In the case of health problems related to indoor air quality, alteration of the environment or protection of the patient from it are necessary components of the treatment plan. The first step in proper medical treatment of indoor air-related illness is to suspect the diagnosis. Sick individuals may present with a variety of symptoms. These are often the same as symptoms seen with other commonly occurring illnesses, such as the flu, common cold, and non-building-related rhinitis, sinusitis, and asthma. For this reason and because objective medical findings
404

are often scanty, diagnosis depends to a large extent on history-both medical and exposure histories. This approach is no different from that applied to other medical conditions, except that the exposure history critical to diagnosis is often more difficult to come by. Reasons include lack of specific training of health care providers and, in some cases, unwillingness on the part of employers to provide the necessary information. For the health care provider faced with a patient with suspected indoor- air-related health problems, it is important to bear in mind that measured levels of contaminants in buildings may be misleading. Measured levels may vary over time or from one part of a building or another; thus a given measurement may reflect a "best case" scenario that is not representative of usual exposures. For the most part, exposure limits established by Federal or state law apply to the industrial sector. Levels of contaminants lower than those allowed by the Occupational Safety and Health Administration (OSHA) and state regulatory agencies can cause problems. More recently, OSHA, the EPA, and the American Society of Heating, Refrigeration, and Air Conditioning Engineers have turned attention to the development of standards that apply to indoor air in the nonindustrial sector. Also, effects of individual air quality problems in a building may be additive. For example, particulate matter can adsorb VOCs. Excess heat can add to the central nervous system effects of VOCs, enhancing such symptoms as fatigue and headache. There appears to be an interaction between chemosensory neuroreceptors in the body and thermosensory neuroreceptors, so that cooler temperatures are associated with less chemical sensitivity.'8 Finally, certain building occupants are likely to be particularly vulnerable to airborne contaminants. For example, individuals taking steroids or chemotherapeutic drugs are at increased risk for serious infection from molds and fungi growing in water-damaged walls or carpeting.
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Having recognized the problem, how do health care providers working together with employers and those responsible for designing, building, and maintaining buildings fix or prevent it? Several professional disciplines must be involved, including industrial hygienists to examine airborne contaminants, microbiologists when mold or fungal contamination is in question, engineers to examine the design and operation of the HVAC system, and physicians experienced in occupational and environmental medicine. Additionally, the aid of a psychologist with experience in building-related problems is often essential to ultimate resolution of the problem and a return to "business as usual." Psychological consultation may be needed on both an organizational and an individual level. If an indoor air quality problem does develop in a building, it should receive prompt attention from those responsible for fixing it which may include management perI sonnel, building owners, or building managers. The longer recognition and correction of the problem takes, the greater the likelihood that symptoms will become chronic. Although the symptoms on their surface may seem trivial, together or alone they are enough to interfere with normal productivity and cause resentment directed at employers for real or perceived inattention to the problem, resulting in distrust and an "us-them" situation. The latter may be more difficult to resolve than the original indoor air quality problem. (See "Communications: A Critical Link in the Management of Indoor Air Quality," p. 406.)
Prevention strategies. The principal factors causally related to poor indoor air quality have been identified by NIOSH and others, as have solutions.,8 Interventions range from preconstruction intervention to "after-thefact" legal strategies. (See Box on page 409.)

ning that takes into account factors that will affect air quality once construction is completed. The design and location of the HVAC system is critically important to the xvell-being of a building. Careful attention should be paid to location of air intake units and their relationship to sources of pollution. For example, rooftop units may pull into the HVAC system pigeon and other bird droppings as part of the outside "fresh" air brought into the building, increasing the risk for psittacosis infection in building occupants. Intake units located near parking lots, loading docks, or busy highways increase the likelihood of drawing into the building vehicular exhaust, carbon monoxide, VOCs, and particulates. Decisions must also be made with regard to amount of fresh air intake and the handling of return air. At present, the rec_ ommended minimum amount of fresh air supply for buildings is 15 cubic feet per minute (cfm) per person in a

sedentary, nonsmoking environment, with a recommended range of 15 cfm/person to 20

cfm/person.' Meeting
this standard does not necessarily insure adequate air quality, however. Ventilation requirements are determined by a variety of factors. These include the number of occupants in a given space, climate variables, and the concentration of airborne chemicals and other pollutants. Some data suggest that increasing ventilation rates above a baseline of 10 liters per second per person does not result in substantial reduction in complaints of indoor air quality-related symptoms.22 On the other hand, if baseline rates of fresh air intake are below 10 liters per second per person, increases in ventilation rate are associated with reduction in building occupants' symptoms. Recirculated indoor air is handled by structural ductwork or through a space (plenum) above a dropped ceiling, with ducted air return being the generally preferred alternative by those knowledgeable in HVAC system design and operation. Careful consideration should be given to whether the ductwork is to be insulated and if so, with what. For example, insulating ducts with fibrous glass material has been associated with indoor contamination with microscopic fibers, resulting in dermatitis and upper respiratory tract irritation among exposed occupants. Design specifications for HVAC systems should include attention to factors that will minimize moisture
*

Butilding design and construction. Before a building is constructed or renovated, architects responsible for building design, engineers responsible for such things as HVAC system design and operation, and building contractors responsible for actual construction must work together. This formal communication will facilitate rational planP' L 13 1. C H EA LLT I I R L 1' ()R T S * S t 'T 'L

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to facilitate removal of dirt and other residue from shoes prior to building entry (metal grates, for example). Proper landscaping will allow drainage of moisture away from the base of the building and minimize the likelihood of xvater damage and secondary pest and mold/fungal infestation and the need for pesticide treatment later.'8 Before the building is occupied, there should be a "test drive" of the HVAC system so that defects can be corrected before rather than after the fact of indoor air quality problems. In addition, sufficient time should be allowed for off-gasing from construction and painting/refinishing materials before employees are allowed back into the building or work area. If work is being done close to building occupants, these occupants should be removed from the building or work areas should be rigorously isolated to protect occupants. Building maintenance. Essential to a healthy indoor environment is a proactive and rigorous operations and maintenance program.

accumulation, which creates a breeding ground for

Provision must be made for reasonable and consistent control of both temperature and relative humidity. Extremes of either have adverse effects on building occupants, both directly and indirectly. Warm humid air encourages the growth of microorganisms, including house dust mites. Air that is too dry may cause dry, itchy skin and eye and upper respiratory tract irritation. Excessive variability in temperature is uncomfortable and distracting for building occupants. Careful attention to roof and window design and construction is needed to minimize moisture accumulation on the roof and leakage around and glare from windows. The building envelope should be constructed so that there is slight positive pressure inside the building. Upholstered interior furnishings and carpeting should be kept to a minimum because of their role as dust collectors and VOC emitters. Attention should be given to devices

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Mlaintenance and custodial work must be performed after normal work hours except in the event of an emergency. Careful and planned maintenance wvill keep the need for emergency repairs to a minimum. If emergency repair work is needed, it must be performed with appropriate isolation of the work area. The HVAC system must be well maintained inspected and cleaned on a prescheduled and periodic basis and repaired as needed. If maintenance is inadequate, problems that may arise again include growth and dissemination of microbial agents from water reservoirs or water-damaged areas as well as the dissemination of irritant dust through supply air from the HVAC system. Dust must be carefully removed from horizontal surfaces, and vacuuming of carpets done with efficient filters and in a manner least likely to stir up dust. Cleaning agents should be chosen not only with cost in mind but also with consideration of the potential toxic effects.

Promoting Good Indoor Air Quality

Building design and construction

Legal safeguards

Quality of indoor air

Building maintenance

Building occupants

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Building occupants. Building occupants themselves have an important role to play in maintaining clean air. Building occupants should keep work areas tidy so that it is easier for them to be cleaned by custodial staff. A no smoking policy is imperative. Smoking outside but near the building should be prohibited because tobacco smoke can be drawn into the building envelope. Wearing of perfumes to work should be minimized. Cooking should be restricted to limited and x.Nell ventilated areas. Legatl strategies. Wlhilc the commiion sense approach to the pirollem of poor indoor air (dUality is to do things right in the first place. another xN7av of increasin"g the likelihood that preventive sleps will be taken and that identifiecd problems will be swiftly and effective
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remediated is to resort to legal strategies as a "court of last resort." Potential tenants of commercial or residential properties might insert into the lease a clause that requires clean indoor air, with specification of minimum standards to be met and penalties for failure to comply or respond promptly in the event of an accident. Buildings have been declared "products" in some courts of law, so product liability laws mLVay appkI.'-; Deter- nilai_ tion of n egligen ce o n the pairt of resoionsible parties in suchi ar-cas as b)tuilcding( alnd( HVAC CleSign-, bUilding and
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socioeconomic groups in the United States. It is a problem that affects all members of society, and health care professionals alone can not fix it. Fortunately, indoor air quality-related illness is preventable. The principal causes have been identified. Strategies for resolution and prevention have been developed. Although often expensive in the short term, their implementation is likely to be cost-effective in the long run. But that will require political and financial commitment and action from a variety of forces. Education of all potentially affected parties is critical. The problem of poor indoor air quality and its related health effects is not going away. It will only increase as time goes on if action is not taken today. The best defense in this case is truly a good offense.
Dr. Oliver is President of Occupational Health Initiatives, an Associate Physician at Massachusetts General Hospital, Boston, and an Assistant Clinical Professor of Medicine at Harvard Medical School. Dr. Shackleton is a clinical and occupational health psychologist, a Clinical Associate in Psychology/Psychiatry, Massachusetts General Hospital, and an Instructor at Harvard Medical School.

ated a health risk or resulted in injury. If corrective action is not taken, legal action against those responsible may serve to prevent reoccurrence of similar problems in the future.
SUM MARY

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Health effects of poor indoor air quality are becoming increasingly important as a public health problem. At-risk populations include virtually all age, occupational, and
References
1. Fraser DW, Tsai TR, Orenstein W, Parkin WE, Beecham HJ, Sharrar RG, et al. Legionnaires' disease: description of an epidemic of pneumonia. N Engl J Med 1977;297:1189-97. 2. Menzies D, Bourbeau J. Building-related illnesses: current concepts. N Engl J Med 1997;337:1524-31. 3. Hoffman RE, Wood RC, Kreiss K. Building-related asthma in Denver office workers. Am J Public Health 993;83:89-93. 4. Arnow PM, Fink JN, Schlueter DP, Barboriak JJ, Mallison G, Said Si, et al. Early detection of hypersensitivity pneumonitis in office workers. Am J Med 1978;64:236-42. 5. Global Initiative for Asthma. Global strategy for asthma management and prevention. NHLBI/WHO Workshop Report. Bethesda (MD): National Heart Lung and Blood Institute (US); 1995 Jan. Pub. No.: 95-3659. 6. Mannino DM, Homa DM, Pertowski CA, Ashizawa A, Nixon LL, Johnson CA, et al. Surveillance for asthma-United States, 1960-1995. MMWR CDC Surveill Summ 1998;47:1-27. 7. Indoor air quality: selected references. Cincinnati (OH): National Institute for Occupational Safety and Health (US); 1989 Sep. 8. Burge S, Hedge A, Wilson S, Bass JH, Robertson A. Sick building syndrome: a study of 4,373 office workers. Ann Occup Hyg 1987;31:493504. 9. Whorton MD, Larson Sr, Gordon NJ, Morgan RW. Investigations and work-up of tight building syndrome. J Occup Med 1987;29:142-6. 10. SametJM, Marbury MC, SpenglerJD. Health effects and sources of indoor air pollution. Part 1: state of art. Am Rev Respir Dis 1987; 136: 1486-1508. I1. Current estimates from the National Health Interview Survey, 1994. Vital Health Stat 1995;10(193). 12. Mitchell FL, editor. Agency for Toxic Substances Disease Registry (US).

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